The genus Adonis (Ranunculaceae) contains about 30 species and is widespread in Eurasia. This genus contains some species of pharmaceutical and ornamental interest, yet a phylogenetic framework for understanding its evolution is still lacking. It has been hypothesized that Adonis originated in the Qinghai-Tibet Plateau (QTP) and migrated out of the QTP through three dispersal routes. This biogeographical hypothesis has never been tested using molecular data. Using nine plastid and nuclear DNA regions, we first reconstructed a robust phylogenetic framework for Adonis with its currently recognized 31 species. We then inferred evolutionary patterns of morphological characters, estimated divergence times, and reconstructed ancestral ranges. Our results show that Adonis and its two subgenera A. subg. Adonis and subg. Adonanthe are monophyletic with strong support. Among the four non-monotypic sections, only A. sect. Adonanthe is recognized as monophyletic. Habit, basal leaf, pollen, and carpel carry a strong phylogenetic signal in Adonis, while achene, beak shape, and beak length exhibit relatively higher levels of evolutionary flexibility. Adonis originated in the QTP in the Oligocene (ca. 30 Ma) and subsequently dispersed into the Irano-Turanian region in the early Miocene (ca. 20 Ma). In Adonis, four out-of-QTP dispersal routes were recognized from the late Miocene to the Pliocene. This study provides the first comprehensive phylogeny for Adonis and highlights the indispensable role of the QTP uplift and associated climatic events in shaping the current distribution and endemism of Adonis, hence contributing to the knowledge on the historical biogeography of plants in Eurasia.